Planta Med 2020; 86(03): 198-204
DOI: 10.1055/a-1078-7860
Biological and Pharmacological Activity
Original Papers
Georg Thieme Verlag KG Stuttgart · New York

Suppressive Effects of Hot-water Extract of Magnolia obovata on Clostridium perfringens Enterotoxin-induced Cytotoxicity in Human Intestinal Caco-2 Cells

Takeshi Kawahara
1   Academic Assembly School of Science and Technology, Institute of Agriculture, Shinshu University
,
Kotomi Fujii
1   Academic Assembly School of Science and Technology, Institute of Agriculture, Shinshu University
,
Kouki Nakajima
1   Academic Assembly School of Science and Technology, Institute of Agriculture, Shinshu University
,
Rikuri Fujii
1   Academic Assembly School of Science and Technology, Institute of Agriculture, Shinshu University
,
Shuichiro Inagaki
2   Department of Health and Nutrition, Faculty of Health and Nutrition, Osaka Shoin Womenʼs University
,
Kunio Hara
3   Kiso Town Resources Institute
,
Hisako Yasui
3   Kiso Town Resources Institute
› Author Affiliations
Further Information

Publication History

received 15 July 2019
revised 02 December 2019

accepted 06 December 2019

Publication Date:
02 January 2020 (online)

Abstract

The physiological functions of the leaves of Japanese big-leaf magnolia (Magnolia obovata) against enterotoxins produced by foodborne pathogens remain unclear. In this study, we evaluated the protective effects of M. obovata leaf extract (MLE) against the cytotoxicity of Clostridium perfringens enterotoxin (CPE), which causes the symptoms of C. perfringens type A food poisoning. The protective effects of MLE against CPE-induced cytotoxicity were evaluated in human intestinal epithelial Caco-2 cells. Pre-treatment with MLE significantly suppressed the cytotoxicity induced by CPE in undifferentiated and differentiated human intestinal Caco-2 cells at a pH range of 4.0 – 7.0. This CPE-suppressive effect was due to a hydrophilic sugar-containing compound without phenolic and protein structures but not the hydrophobic biologically active neolignans, honokiol and magnolol. MLE had a protective effect against cytotoxicity caused by type A C. perfringens. Our results provide novel insight regarding the usage of M. obovata in managing food poisoning.

Supporting Information

 
  • References

  • 1 Hu Y, Qiao J, Zhang X, Ge C. Antimicrobial effect of Magnolia officinalis extract against Staphylococcus aureus . J Sci Food Agric 2011; 91: 1050-1056
  • 2 Jacobo-Salcedo Mdel R, Gonzalez-Espindola LA, Alonso-Castro AJ, Gonzalez-Martinez Mdel R, Domínguez F, Garcia-Carranca A. Antimicrobial activity and cytotoxic effects of Magnolia dealbata and its active compounds. Nat Prod Commun 2011; 6: 1121-1124
  • 3 Sakaue Y, Domon H, Oda M, Takenaka S, Kubo M, Fukuyama Y, Okiji T, Terao Y. Anti-biofilm and bactericidal effects of magnolia bark-derived magnolol and honokiol on Streptococcus mutans . Microbiol Immunol 2016; 60: 10-16
  • 4 Choi WS, Lee TH, Son SJ, Kim TG, Kwon BM, Son HU, Kim SU, Lee SH. Inhibitory effect of obovatol from Magnolia obovata on the Salmonella type III secretion system. J Antibiot (Tokyo) 2017; 70: 1065-1069
  • 5 McClane BA, Robertson SL, Li J. Clostridium perfringens . In: Doyle MP, Buchanan RL. eds. Food Microbiology: Fundamentals and Frontiers. 4th ed. Washington, DC: ASM Press; 2013: 465-489
  • 6 Cosansu S, Juneja VK. Growth of Clostridium perfringens in sous vide cooked ground beef with added grape seed extract. Meat Sci 2018; 143: 252-256
  • 7 McClane BA, Uzal FA, Miyakawa MF, Lyerly D, Wilkins TD. The enterotoxic Clostridia. In: Dworkin M, Falkow S, Rosenburg E, Schleifer H, Stackebrandt E. eds. The Prokaryotes. 3rd ed.. New York: Springer NY Press; 2006: 688-752
  • 8 Freedman JC, Theoret JR, Wisniewski JA, Uzal FA, Rood JI, McClane BA. Clostridium perfringens type A–E toxin plasmids. Res Microbiol 2015; 166: 264-279
  • 9 Chakrabarti G, Zhou X, McClane BA. Death pathways activated in Caco-2 cells by Clostridium perfringens enterotoxin. Infect Immun 2003; 71: 4260-4270
  • 10 Chakrabarti G, McClane BA. The importance of calcium influx, calpain, and calmodulin for the activation of Caco-2 cell death pathways by Clostridium perfringens enterotoxin. Cell Microbiol 2005; 7: 129-146
  • 11 Czeczulin JR, Hanna PC, McClane BA. Cloning, nucleotide sequencing, and expression of the Clostridium perfringens enterotoxin gene in Escherichia coli . Infect Immun 1993; 61: 3429-3439
  • 12 Heikinheimo A, Lindström M, Granum PE, Korkeala H. Humans as reservoir for enterotoxin gene-carrying Clostridium perfringens type A. Emerg Infect Dis 2006; 12: 1724-1729
  • 13 McNamara C, Bedard BA, Weimer AC, Pennise M, Kennedy BS. A Clostridium perfringens outbreak traced to improper cooking of prime rib in Rochester, New York 2011. Food Prot Trends 2014; 34: 392-396
  • 14 Clevers H. The intestinal crypt, a prototype stem cell compartment. Cell 2014; 154: 274-284
  • 15 Crosnier C, Stamataki D, Lewis J. Organizing cell renewal in the intestine: stem cells, signals and combinatorial control. Nat Rev Genet 2006; 7: 349-359
  • 16 Mariadason JM, Rickard KL, Barkla DH, Augenlicht LH, Gibson PR. Divergent phenotypic patterns and commitment to apoptosis of Caco-2 cells during spontaneous and butyrate-induced differentiation. J Cell Physiol 2000; 183: 347-354
  • 17 Kotani A, Kojima S, Hakamata H, Jin D, Kusu F. Determination of honokiol and magnolol by micro HPLC with electrochemical detection and its application to the distribution analysis in branches and leaves of Magnolia obovata . Chem Pharm Bull (Tokyo) 2005; 53: 319-322
  • 18 Zhang WW, Li Y, Wang XQ, Tian F, Cao H, Wang MW, Sun QS. Effects of magnolol and honokiol derived from traditional Chinese herbal remedies on gastrointestinal movement. World J Gastroenterol 2005; 11: 4414-4418
  • 19 Chen CR, Tan R, Qu WM, Wu Z, Wang Y, Urade Y, Huang ZL. Magnolol, a major bioactive constituent of the bark of Magnolia officinalis, exerts antiepileptic effects via the GABA/benzodiazepine receptor complex in mice. Br J Pharmacol 2011; 164: 1534-1546
  • 20 Arora S, Singh S, Piazza GA, Contreras CM, Panyam J, Singh AP. Honokiol: a novel natural agent for cancer prevention and therapy. Curr Mol Med 2012; 12: 1244-1252
  • 21 Hasegawa T, Fukuyama Y, Yamada T, Nakagawa K. Isolation and structure of magnoloside A, a new phenylpropanoid glycoside from Magnolia obovate Thunb. Chem Lett 1988; 17: 163-166
  • 22 Katahira J, Inoue N, Horiguchi Y, Matsuda M, Sugimoto N. Molecular cloning and functional characterization of the receptor for Clostridium perfringens enterotoxin. J Cell Biol 1997; 136: 1239-1247
  • 23 Amasheh M, Schlichter S, Amasheh S, Mankertz J, Zeitz M, Fromm M, Schulzke JD. Quercetin enhances epithelial barrier function and increases claudin-4 expression in Caco-2 cells. J Nutr 2008; 138: 1067-1073
  • 24 Fujita K, Katahira J, Horiguchi Y, Sonoda N, Furuse M, Tsukita S. Clostridium perfringens enterotoxin binds to the second extracellular loop of claudin-3, a tight junction integral membrane protein. FEBS Lett 2000; 476: 258-261
  • 25 Shrestha A, Robertson SL, Garcia J, Beingasser J, McClane BA, Uzal FA. A synthetic peptide corresponding to the extracellular loop 2 region of claudin-4 protects against Clostridium perfringens enterotoxin in vitro and in vivo . Infect Immun 2014; 82: 4778-4788
  • 26 Kokai-Kun JF, Benton K, Wieckowski EU, McClane BA. Identification of a Clostridium perfringens enterotoxin region required for large complex formation and cytotoxicity by random mutagenesis. Infect Immun 1999; 67: 5634-5641
  • 27 Sonoda N, Furuse M, Sasaki H, Yonemura S, Katahira J, Horiguchi Y, Tsukita S. Clostridium perfringens enterotoxin fragment removes specific claudins from tight junction strands: evidence for direct involvement of claudins in tight junction barrier. J Cell Biol 1999; 147: 195-204
  • 28 Veshnyakova A, Protze J, Rossa J, Blasig IE, Krause G, Piontek J. On the interaction of Clostridium perfringens enterotoxin with claudins. Toxins (Basel) 2010; 2: 1336-1356
  • 29 Kimura J, Abe H, Kamitani S, Toshima H, Fukui A, Miyake M, Kamata Y, Sugita-Konishi Y, Yamamoto S, Horiguchi Y. Clostridium perfringens enterotoxin interacts with claudins via electrostatic attraction. J Biol Chem 2010; 285: 401-408
  • 30 Wang G, Paredes-Sabja D, Sarker MR, Green C, Setlow P, Li YQ. Effects of wet heat treatment on the germination of individual spores of Clostridium perfringens . J Appl Microbiol 2012; 113: 824-836
  • 31 Byrne B, Dunne G, Bolton DJ. Thermal inactivation of Bacillus cereus and Clostridium perfringens vegetative cells and spores in pork luncheon roll. Food Microbiol 2006; 23: 803-808
  • 32 Redondo-Solano M, Valenzuela-Martinez C, Cassada DA, Snow DD, Juneja VK, Burson DE, Thippareddi H. Effect of meat ingredients (sodium nitrite and erythorbate) and processing (vacuum storage and packaging atmosphere) on germination and outgrowth of Clostridium perfringens spores in ham during abusive cooling. Food Microbiol 2013; 35: 108-115
  • 33 Myers MI, Sebranek JG, Dickson JS, Shaw AM, Tarte R, Adams KR, Neibuhr S. Implications of decreased nitrite concentrations on Clostridium perfringens outgrowth during cooling of ready-to-eat meats. J Food Prot 2016; 79: 153-156
  • 34 Akhtar S, Paredes-Sabja D, Sarker MR. Inhibitory effects of polyphosphates on Clostridium perfringens growth, sporulation and spore outgrowth. Food Microbiol 2008; 25: 802-808
  • 35 Unlu M, Ergene E, Unlu GV, Zeytinoglu HS, Vural N. Composition, antimicrobial activity and in vitro cytotoxicity of essential oil from Cinnamomum zeylanicum Blume (Lauraceae). Food Chem Toxicol 2010; 48: 3274-3280
  • 36 Udompijitkul P, Paredes-Sabja D, Sarker MR. Inhibitory effects of nisin against Clostridium perfringens food poisoning and nonfood-borne isolates. J Food Sci 2012; 77: M51-M56